Spatial sorting may explain evolutionary dynamics of wing polymorphism in pygmy grasshoppers

Wing polymorphism in insects provides a good model system for investigating evolutionary dynamics and population divergence in dispersal‐enhancing traits. This study investigates the contribution of divergent selection, trade‐offs, behaviour and spatial sorting to the evolutionary dynamics of wing polymorphism in the pygmy grasshopper Tetrix subulata (Tetrigidae: Orthoptera). We use data for > 2800 wild‐caught individuals from 13 populations and demonstrate that the incidence of the long‐winged (macropterous) morph is higher and changes faster between years in disturbed habitats characterized by succession than in stable habitats. Common garden and mother‐offspring resemblance studies indicate that variation among populations and families is genetically determined and not influenced to any important degree by developmental plasticity in response to maternal condition, rearing density or individual growth rate. Performance trials show that only the macropterous morph is capable of flight and that propensity to fly differs according to environment. Mark–recapture data reveal no difference in the distance moved between free‐ranging long‐ and short‐winged individuals. There is no consistent difference across populations and years in number of hatchlings produced by long‐ and shorter‐winged females. Our findings suggest that the variable frequency of the long‐winged morph among and within pygmy grasshopper populations may reflect evolutionary modifications driven by spatial sorting due to phenotype‐ and habitat type–dependent emigration and immigration.     

Trade‐offs to flight capability in Gryllus firmus: the influence of whole‐organism respiration rate on fitness

Wing dimorphism, where some macropterous long‐winged (LW) individuals can fly whereas micropterous short‐winged (SW) individuals cannot, is common in insects and believed to be maintained in part by trade‐offs between flight capability and reproductive traits. In this paper we examine differences in whole‐organism respiration rate between wing morphs of the sand cricket Gryllus firmus. We hypothesized that maintenance of the flight apparatus would result in elevated CO₂ respired because of the high metabolic cost of these tissues, which, in turn, constrain resources available for egg production in females. As the trade‐off involves calling behaviour in males, we predicted no equivalent constraint on organ development in this sex. We found female macropters (particularly older crickets) had significantly higher residual respiration rates than micropters. In males, we found only marginal differences between wing morphs. In both sexes there was a highly significant effect of flight muscles status on residual respiration rate, individuals with functional muscles having higher respiration rates. Both female and male macropters had significantly smaller gonads than micropters. Whole‐organism residual respiration rate was negatively correlated with fecundity: macropterous females with high respiration rates had smaller gonads compared with macropterous females with lower respiration rates.     

Density‐dependent sex‐biased development of macroptery in a water strider

In wing‐polymorphic insects, wing morphs differ not only in dispersal capability but also in life history traits because of trade‐offs between flight capability and reproduction. When the fitness benefits and costs of producing wings differ between males and females, sex‐specific trade‐offs can result in sex differences in the frequency of long‐winged individuals. Furthermore, the social environment during development affects sex differences in wing development, but few empirical tests of this phenomenon have been performed to date. Here, I used the wing‐dimorphic water strider Tenagogerris euphrosyne to test how rearing density and sex ratio affect the sex‐specific development of long‐winged dispersing morphs (i.e., sex‐specific macroptery). I also used a full‐sib, split‐family breeding design to assess genetic effects on density‐dependent, sex‐specific macroptery. I reared water strider nymphs at either high or low densities and measured their wing development. I found that long‐winged morphs developed more frequently in males than in females when individuals were reared in a high‐density environment. However, the frequency of long‐winged morphs was not biased according to sex when individuals were reared in a low‐density environment. In addition, full‐sib males and females showed similar macroptery incidence rates at low nymphal density, whereas the macroptery incidence rates differed between full‐sib males and females at high nymphal density. Thus complex gene‐by‐environment‐by‐sex interactions may explain the density‐specific levels of sex bias in macroptery, although this interpretation should be treated with some caution. Overall, my study provides empirical evidence for density‐specific, sex‐biased wing development. My findings suggest that social factors as well as abiotic factors can be important in determining sex‐biased wing development in insects.     

Seasonal differences in body mass and circulating metabolites in a wing‐dimorphic pygmy grasshopper: implications for life history?

1. Functional wing polymorphism in insects is an intriguing topic, especially with respect to the adaptive advantage of each wing morph. The common pygmy grasshopper in Germany, Tetrix subulata, displays wing polymorphism skewed towards macropterous (LW) individuals capable of flight. Furthermore, T. subulata is known to undergo adult diapause in winter and reproduce in spring. 2. Morphometric and biochemical parameters were examined in field‐collected grasshoppers during autumn and spring to obtain a ‘snapshot’ from the same/one cohort of grasshoppers in the wild. 3. Flight muscles are largely reduced in brachypterous (SW) specimens, whereas they are well developed in LW individuals. Body mass measurements indicated gain in female T. subulata in spring, especially in LW morphs, which could be attributed to increased reproductive activity (egg production). 4. Metabolic fuel in haemolymph is differentially distributed in autumn: the concentration of lipids is highest in males, while carbohydrates are most abundant in LW specimens. The metabolic data imply that dispersal in T. subulata is predominantly in autumn, by flight in the case of LW specimens and by hopping/walking in males. 5. The season seems to be an important factor for the reproductive versus dispersal trade‐off in this species. Moreover, this study shows that morphological differences in T. subulata individuals are reflected in physiological differences that may ultimately affect behaviour and ecology.     

Variation in wing dimorphism of oriental mole cricket Gryllotalpa orientalis: Comparative study in Okinawa and Hyogo populations

The oriental mole cricket Gryllotalpa orientalis exhibits variation in wing dimorphism. In an Okinawa population, no short‐winged individuals were observed, and wing dimorphism has not been detected. Flight behavior of G. orientalis was observed from April to October in Okinawa. In contrast, a Hyogo population exhibited seasonal wing dimorphism and long‐winged individuals appear from June to September. The flight period of the long‐winged morph coincided with this period. Short‐winged individuals appeared from September to the following June and they never fly. Both populations showed univoltine life cycles. Considering the possible flight period, wing pattern and life cycle of mole crickets in these two areas, it is presumed that flightlessness is expected to arise when adults can not experience suitable temperatures for flight activity.     

The trade‐off to macroptery in the cricket Gryllus firmus: a path analysis in males

Among the Orthoptera, wing dimorphism, where one morph is long‐winged and flight capable while the other is short‐winged and flight incapable, is common and believed to be maintained in populations due to trade‐offs to flight capability. In males, macropterous individuals call less than micropterous individuals and as a consequence obtain fewer matings. This trade‐off is hypothesized to be mediated by the energetic costs of calling. In this paper we report results for a path analysis examining lipid weight and DLM (dorso longitudinal muscle) condition of male Gryllus firmus. We found that as DLM condition changes from a nonfunctional to a functional state, call duration decreases, and as lipid weight increases, call duration increases. The most important linked path was wing morph → DLM condition → call duration. This model is consistent with the prediction that the trade‐off between wing morph and call duration is mediated via DLM and lipid stores.     

Wing dimorphism in the migratory locust,Locusta migratoria: differentiation of wing morph and phase polyphenism

A short‐winged morph was recently discovered in the migratory locust, Locusta migratoria. It is different from the normal, long‐winged morph not only in forewing length but also in hind femur length, displaying a dimorphism. To understand the significance of this dimorphism, other morphological characters were compared between the two morphs, and the time of differentiation of wing‐pad length was investigated. Wing weights were heavier in the long‐winged morph than in the short‐winged morph. This result showed that the short‐winged morph is not formed by a failure of wing expansion. No obvious morph‐specific differences were observed in wing venation, but wing allometry studies indicated that the distal areas of the fore‐ and hindwings were disproportionally reduced in the short‐winged morph compared to the long‐winged morph. The morphological differentiation of the wing pad between the two morphs was observed at the penultimate nymphal stage. The flight muscle was well developed in the two morphs, and no sign of flight muscle histolysis was detected in either morph after adult emergence. An analysis of adult body dimensions suggested that the density‐dependent phase shifts known for the long‐winged morph of this locust were also exhibited by the short‐winged morph, demonstrating that these shifts are not specific to the migratory long‐winged morph.     

Relationship between morphology,dispersal and habitat distribution in three species of Libellula (Odonata: Anisoptera)

Morphology is an important determinant of flight performance and can shape species’ dispersal behaviour. This study contrasted the morphology of flight-related structures in dragonfly species with different dispersal behaviours to gain insights into the relationship between morphology and dispersal behaviour. Specifically, wing size, wing shape and thorax size were compared in three co-occurring species from different clades within the genus Libellula (Odonata: Anisoptera: Libellulidae) to assess how these morphological traits are related to differences in dispersal behaviour and to how broadly their larvae occur across a habitat gradient. Two species had broad larval habitat distributions as well as high rates and distances of dispersal. These two species had relatively larger wings and thoraces than the third species, which was found only in permanent lakes and had limited dispersal. The hind-wings of more dispersive species also had lower aspect ratios and a relatively wider basal portion of the wing than the less dispersive species. Broad hind-wings may facilitate the use of gliding flight and reduce the energetic costs of dispersal. Determining the morphological traits associated with alternative dispersal behaviours may be a useful tool to assess the differential dispersal capacities of species or populations.     

The cost of being able to fly: a study of wing polymorphism in two species of crickets

Summary The widespread occurrence of wing polymorphisms in insects suggests that the possession of wings and ability to fly adversely affect components of the insect's life characteristics that contribute to its Darwinian fitness. This hypothesis was tested by an analysis of the differences in life history parameters of the macropterous and micropterous morphs of the two cricket species G. firmus and A. fasciatus. In both species there were no differences in development time or adult survival between the two morphs. Significant differences in head width were not consistent between the two species but in both sexes of G. firmus and females of A. fasciatus (insufficient males for analysis) long-winged individuals weighed more than short-winged individuals with the same head width. In both species egg production is delayed in macropterous females. The cumulative fecundity of the micropterous morph is greater than the macropterous morph in both species but only in G. firmus is the difference statistically significant. A. fasciatus frequently loose their wings but no such loss has been observed in G. firmus. There is a significant increase in egg production after the loss of the wings. These results are in accord with those of Tanaka (1976) for the cricket, Pteronemobius taprobanensis.Breeding experiments indicate that in G. firmus the wing polymorphism is under genetic control. The decrease in fecundity is sufficiently large that genotypes producing only macropterous offspring could only persist in highly unstable environments where continuous dispersal was imperative for survival. However, the reproductive cost of a genotype producing a small percentage of macropterous individuals is slight. The fitness that accrues to a genotype producing a few dispersing offspring is likely to offset the small reproductive cost and hence wing polymorphisms should be favoured.     

Similarity in temporal variation in sex‐biased dispersal over short and long distances in the dark‐eyed junco,Junco hyemalis

Patterns of sex‐biased dispersal (SBD) are typically consistent within taxa, for example female‐biased in birds and male‐biased in mammals, leading to theories about the evolutionary pressures that lead to SBD. However, generalizations about the evolution of sex biases tend to overlook that dispersal is mediated by ecological factors that vary over time. We examined potential temporal variation in between‐ and within‐population dispersal over an 11‐year period in a bird, the dark‐eyed junco (Junco hyemalis). We measured between‐population dispersal patterns using genetic assignment indices and found yearly variation in which sex was more likely to have immigrated. When we measured within‐population spatial genetic structure and mark–recapture dispersal distances, we typically found yearly SBD patterns that mirrored between‐population dispersal, indicating common eco‐evolutionary causes despite expected differences due to the scale of dispersal. However, in years without detectable between‐population sex biases, we found genetic similarity between nearby males within our population. This suggests that, in certain circumstances, ecological pressures may act on within‐population dispersal without affecting dispersal between populations. Alternatively, current analytical tools may be better able to detect within‐population SBD. Future work will investigate potential causes of the observed temporal variation in dispersal patterns and whether they have greater effects on within‐population dispersal.     

Do smaller islands host younger populations? A case study on metapopulations of three carabid species

Aims To test a new concept for island ecology and metapopulation studies: if population persistence is a result of colonization and extinction processes, one would expect remarkable variability in the age of neighbouring populations – there would be both old and young (recently established) populations. Location The lake Mamry archipelago, Poland. Methods Forty trap transects with a total of 114 Barber traps were operating from June to September in 1997 and in 1998. The traps (0.5‐L plastic beakers, mouth diameter 120 mm, with a 20 × 20 cm wooden roof) were placed by applying a stratified sampling design into 13 habitat types on the 16 islands and two mainland sites. The frequency of macropterous individuals in wing‐dimorphic populations of three carabid species (Pterostichus melanarius, P. anthracinus and Carabus granulatus) was used as an indicator of population ‘age’. Results The frequency of macropterous individuals in the populations varied from 0% to 100% for P. melanarius (18.5% on average), from 0% to 91% for P. anthracinus (12.6%) and from 0% to 29% for C. granulatus (8.9%). Populations hosted more long‐winged individuals (and were therefore interpreted as being younger) on smaller islands, compared with those inhabiting large islands and the mainland sites. The results also revealed that the viability of the populations of the autumn‐breeding P. melanarius might be more affected by population size than that of the two studied spring breeders. Island connectivity did not have a significant effect on the frequency of macropterous individuals in the studied populations. Main conclusions The inverse relationship between the proportion of macropterous individuals and island size contrasts with the accepted theory of dispersal, which assumes that there is selection against dispersal on small islands. A regression analysis for population age and habitat characteristics reveals the extinction probability of a given population. I suggest that investigations based on variability in population age can help in studies of colonization–extinction processes that would otherwise face logistic and methodological obstacles.     

Antagonistic and reinforcing pleiotropy: a study of differences in development time in wing dimorphic insects

Morphological dimorphisms are found in many different taxa. Wing dimorphism in insects, in which some individuals possess wings and associated flight muscles and are thus volant while others lack a functional flight apparatus and are thus flightless, is a typical example of such types of dimorphisms. It has been extensively studied and such studies have demonstrated that the volant form, although possessing the advantage of flight capability, suffers a fitness cost in a delay in the onset of reproduction after emergence into the adult form and a reduced fecundity. Previous comparative analyses have suggested that there is no consistent trend for development time (hatching to adult) to differ between the two morphs. The present study analyses the phenotypic and genetic correlations between development time and wing morph in the cricket Gryllus firmus. It is shown that the macropterous (volant) morph develops faster than the micropterous (flightless morph). This trade-off is manifested at both thephenotypic and genetic level. Further, a comparative analysis shows that the same phenotypic trade-off is generally found in other Orthopteran species so far studied, but in other orders the micropterous morph develops faster. Provided that the phenotypic trade-off is genetically based, in the Orthoptera the fitness advantage of the earlier onset of reproduction in micropterous females is offset by the extended development time (antagonistic pleiotropy). However, in other orders there is reinforcing pleiotropy in that the micropterous females develop faster and reproduce sooner than the macropterous morph. These results highlight the complexity of fitness interactions and the need to study a phenomenon across several taxa.     

Dispersal capability in a habitat specialist bush cricket: the role of population density and habitat moisture

1. In fragmented landscapes many insect species depend on a regular exchange of individuals between subpopulations to ensure the persistence of the population. Thus, the ability to disperse is of particular relevance. 2. However, in some insect species mobility is not a fixed trait. Hence, knowing the causes of phenotypic plasticity is of great importance when evaluating whether a species is able to survive in fragmented landscapes or not. 3. A multi‐year field study was conducted to identify possible causes of macroptery in the wing‐dimorphic habitat specialist Metrioptera brachyptera L. and to quantify its dispersal capability (% macropters). Therefore, 746 individuals of the species were caught on 135 plots. Additionally, environmental variables that possibly induce the development of macropters (population density and habitat moisture) were recorded. 4. Dispersal capability of M. brachyptera was very low. Less than 3% were long‐winged. The statistical analysis revealed that the proportion of long‐winged M. brachyptera was strongly correlated with high bush‐cricket densities and not with habitat moisture. 5. The low dispersal capability of M. brachyptera leads to the conclusion that individual exchange between isolated populations is limited or even impossible. Habitat specialists, like M. brachyptera, may thus be unable to respond to rapid changes in the availability of suitable habitats by dispersing, and hence may be especially dependent on habitat management activities that promote the long‐term stability of existing habitat patches.     

Sex‐specific graphs: Relating group‐specific topology to demographic and landscape data

Sex‐specific genetic structure is a commonly observed pattern among vertebrate species. Facing differential selective pressures, individuals may adopt sex‐specific life history traits that ultimately shape genetic variation among populations. Although differential dispersal dynamics are commonly detected in the literature, few studies have used genetic structure to investigate sex‐specific functional connectivity. The recent use of graph theoretic approaches in landscape genetics has demonstrated network capacities to describe complex system behaviours where network topology represents genetic interaction among subunits. Here, we partition the overall genetic structure into sex‐specific graphs, revealing different male and female dispersal dynamics of a fisher (Pekania [Martes] pennanti) metapopulation in southern Ontario. Our analyses based on network topologies supported the hypothesis of male‐biased dispersal. Furthermore, we demonstrated that the effect of the landscape, identified at the population level, could be partitioned among sex‐specific strata. We found that female connectivity was negatively correlated with snow depth, whereas connectivity among males was not. Our findings underscore the potential of conducting sex‐specific analysis by identifying landscape elements or configuration that differentially promotes or impedes functional connectivity between sexes, revealing processes that may otherwise remain cryptic. We propose that the sex‐specific graph approach would be applicable to other vagile species where differential sex‐specific processes are expected to occur.     

The sex chromosome system can influence the evolution of sex‐biased dispersal

Sex‐biased dispersal is a much‐discussed feature in literature on dispersal. Diverse hypotheses have been proposed to explain the evolution of sex‐biased dispersal, a difference in dispersal rate or dispersal distance between males and females. An early hypothesis has indicated that it may rely on the difference in sex chromosomes between males and females. However, this proposal was quickly rejected without a real assessment. We propose a new perspective on this hypothesis by investigating the evolution of sex‐biased dispersal when dispersal genes are sex‐linked, that is when they are located on the sex chromosomes. We show that individuals of the heterogametic sex disperse relatively more than do individuals of the homogametic sex when dispersal genes are sex‐linked rather than autosomal. Although such a sex‐biased dispersal towards the heterogametic sex is always observed in monogamous species, the mating system and the location of dispersal genes interact to modulate sex‐biased dispersal in monandry and polyandry. In the context of the multicausality of dispersal, we suggest that sex‐linked dispersal genes can influence the evolution of sex‐biased dispersal.     

Locomotor activity in adult Pyrrhocoris apterus (Heteroptera) in relation to sex, physiological status and wing dimorphism

The pattern of locomotor (walking) activity was studied in adult males and females of short‐winged (brachypterous) and long‐winged (macropterous) morph of the flightless bug Pyrrhocoris apterus (Linnaeus) (Heteroptera: Pyrrhocoridae) under constant laboratory conditions. Walking activity was measured with a computerized video system and analysed with respect to sex, physiological status (reproduction, diapause and reproductive arrest of non‐diapause type) and wing dimorphism of the bugs. The largest duration was observed in the macropterous females with reproductive arrest of non‐diapause type (average 6 h per day) and the shortest duration in diapausing brachypterous females and males (average less than 2 h per day). This was reflected also in the overall time spent by walking during the first 14 days after imaginal ecdysis. The time spent by walking significantly increased in the macropterous morph as the bugs aged, whereas in diapausing brachypters the time spent by walking decreased with age. No linear relationship between walking activity and age was found in reproductive brachypterous morph. The bugs of all experimental groups moved mostly during the photophase and were almost inactive during the scotophase. Thus, walking activity in P. apterus is diurnal, irrespective of the wing morph, physiological status, sex and age. Contrary to the macropterous morph, where the locomotor activity of females during photophase was significantly higher than in males, no significant differences were found between the locomotor activities of brachypterous males and females. The observed differences in locomotor activity are discussed in relation to different roles of two wing morphs in the life history of this heteropteran.     

Evaluating the life‐history trade‐off between dispersal capability and reproduction in wing dimorphic insects: a meta‐analysis

A life‐history trade‐off exists between flight capability and reproduction in many wing dimorphic insects: a long‐winged morph is flight‐capable at the expense of reproduction, while a short‐winged morph cannot fly, is less mobile, but has greater reproductive output. Using meta‐analyses, I investigated specific questions regarding this trade‐off. The trade‐off in females was expressed primarily as a later onset of egg production and lower fecundity in long‐winged females relative to short‐winged females. Although considerably less work has been done with males, the trade‐off exists for males among traits primarily related to mate acquisition. The trade‐off can potentially be mitigated in males, as long‐winged individuals possess an advantage in traits that can offset the costs of flight capability such as a shorter development time. The strength and direction of trends differed significantly among insect orders, and there was a relationship between the strength and direction of trends with the relative flight capabilities between the morphs. I discuss how the trade‐off might be both under‐ and overestimated in the literature, especially in light of work that has examined two relevant aspects of wing dimorphic species: (1) the effect of flight‐muscle histolysis on reproductive investment; and (2) the performance of actual flight by flight‐capable individuals.     

Characterizing dispersal patterns in a threatened seabird with limited genetic structure

Genetic assignment methods provide an appealing approach for characterizing dispersal patterns on ecological time scales, but require sufficient genetic differentiation to accurately identify migrants and a large enough sample size of migrants to, for example, compare dispersal between sexes or age classes. We demonstrate that assignment methods can be rigorously used to characterize dispersal patterns in a marbled murrelet (Brachyramphus marmoratus) population from central California that numbers approximately 600 individuals and is only moderately differentiated (F_ST～ 0.03) from larger populations to the north. We used coalescent simulations to select a significance level that resulted in a low and approximately equal expected number of type I and II errors and then used this significance level to identify a population of origin for 589 individuals genotyped at 13 microsatellite loci. The proportion of migrants in central California was greatest during winter when 83% of individuals were classified as migrants compared to lower proportions during the breeding (6%) and post‐breeding (8%) seasons. Dispersal was also biased toward young and female individuals, as is typical in birds. Migrants were rarely members of parent‐offspring pairs, suggesting that they contributed few young to the central California population. A greater number of migrants than expected under equilibrium conditions, a lack of individuals with mixed ancestry, and a small number of potential source populations (two), likely allowed us to use assignment methods to rigorously characterize dispersal patterns for a population that was larger and less differentiated than typically thought required for the identification of migrants.     

Flight threshold, wing muscle histolysis, and alary polymorphism: correlated traits for dispersal tendency in the Gerridae

ABSTRACT. 1. This paper tests the hypothesis that selection for dispersal ability within a species influences not only the occurrence and extent of wing reduction but also the tendency or ability of the macropterous individuals to fly.
2. Flight thresholds of four species of waterstriders (Hemiptera; Gerridae) were assessed using a tethered flight technique. The species tested varied from monomorphic macropterous ( Limnoporus dissortis Drake and Harris), through seasonally polymorphic ( Gerris comatus Drake and Hottes and G. buenoi Kirkaldy), to primarily apterous ( G.remigis Say).
3. Condition of the indirect, mesothoracic flight muscles, and presence or absence of mature or developing eggs (for females) were determined by dissection of all individuals immediately following flight testing. Only individuals with normal muscles were included in the analysis of flight thresholds.
4. Comparisons among species revealed that average flight threshold and extent of flight muscle histolysis were negatively associated with the proportion of macropterous individuals. Wing reduction was also associated with significant seasonal variation in flight threshold, particularly among females.
5. These results support our initial hypothesis, and further indicate that, within the Gerridae, dispersal tendency depends not only on the proportion of macropters but also on the dispersal capability of the macropterous individuals.     

Sex‐specific estimates of dispersal show female philopatry and male dispersal in a promiscuous amphibian,the alpine salamander (Salamandra atra)

Amphibians display wide variations in life‐history traits and life cycles that should prove useful to explore the evolution of sex‐biased dispersal, but quantitative data on sex‐specific dispersal patterns are scarce. Here, we focused on Salamandra atra, an endemic alpine species showing peculiar life‐history traits. Strictly terrestrial and viviparous, the species has a promiscuous mating system, and females reproduce only every 3 to 4 years. In the present study, we provide quantitative estimates of asymmetries in male vs. female dispersal using both field‐based (mark–recapture) and genetic approaches (detection of sex‐biased dispersal and estimates of migration rates based on the contrast in genetic structure across sexes and age classes). Our results revealed a high level of gene flow among populations, which stems exclusively from male dispersal. We hypothesize that philopatric females benefit from being familiar with their natal area for the acquisition and defence of an appropriate shelter, while male dispersal has been secondarily favoured by inbreeding avoidance. Together with other studies on amphibians, our results indicate that a species' mating system alone is a poor predictor of sex‐linked differences in dispersal, in particular for promiscuous species. Further studies should focus more directly on the proximate forces that favour or limit dispersal to refine our understanding of the evolution of sex‐biased dispersal in animals.